基于转录组数据揭示4种兜兰的全基因组复制历史

doi:10.11983/CBB21100

植物学报 ›› 2021, Vol. 56 ›› Issue (6): 699-714.DOI: 10.11983/CBB21100

基于转录组数据揭示4种兜兰的全基因组复制历史

王蒙¹, 王婷¹^,², 夏增强¹^,³, 李廷章¹, 金效华⁴, 严岳鸿¹, 陈建兵¹^,^*()

¹深圳市兰科植物保护研究中心, 兰科植物保护与利用国家林业和草原局重点实验室, 深圳 518114
²西南林业大学生物多样性保护学院, 昆明 650224
³中国科学院分子植物科学卓越创新中心, 上海 200032
⁴中国科学院植物研究所, 系统与进化植物学国家重点实验室, 北京 100093

收稿日期:2021-06-22 接受日期:2021-11-24 出版日期:2021-11-01 发布日期:2021-11-24
通讯作者: 陈建兵
作者简介:* E-mail: cjb@cnocc.cn
基金资助:
中央林业改革发展资金(粤财资环[2019]5号)

Revealing the New Whole-genome Duplication Event of Four Paphiopedilum Species Based on Transcriptome Data

Meng Wang¹, Ting Wang¹^,², Zengqiang Xia¹^,³, Tingzhang Li¹, Xiaohua Jin⁴, Yuehong Yan¹, Jianbing Chen¹^,^*()

¹Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, The Orchid Conservation & Research Center of Shenzhen, Shenzhen 518114, China
²College of Biodiversity Conservation, Southwest Forestry University, Kunming 650224, China
³Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai 200032, China
⁴State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China

Received:2021-06-22 Accepted:2021-11-24 Online:2021-11-01 Published:2021-11-24
Contact: Jianbing Chen

1. 附表1 4 种兜兰转录因子家族.pdf(1422KB)

摘要/Abstract

摘要： 多倍化或全基因组复制(WGD)是物种多样性发生的重要驱动力。目前, 在蕨类、菊科以及豆科等类群丰富的植物中已多次报道全基因组复制事件, 而兰科(Orchidaceae)全基因组复制事件报道极少, 与其丰富的物种多样性存在矛盾, 推测与前期样本量小但类群跨度大的研究策略有关。选取染色体数目变异丰富且多样性较高的兜兰属(Paphiopedilum)为兰科植物代表类群, 基于共享数据库中4种兜兰的转录组数据, 采用同义替换率(K_s)、系统发生基因组学以及相对定年的方法分析兜兰属植物是否发生过全基因组复制事件。结果表明, 在4种兜兰中均检测到3次全基因组复制事件, 分别发生在110.17-119.77 Mya (WGD1)、60.95-74.19 Mya (WGD2)和38.19-45.85 Mya (WGD3)。其中, WGD3为新检测到的全基因组复制事件, 推测其发生在杓兰亚科(Cypripedioideae)与姐妹类群分化后, 兜兰属与姐妹类群分化之前。此外, 3次全基因组复制事件发生后优先保留的基因拷贝在功能上多与当时的环境胁迫响应相关, 推测全基因组复制提高了兜兰属植物祖先对当时极端环境变化的适应性。

关键词: 多倍化, 兰科, 杓兰亚科, 适应性演化, 同义替换率

Abstract: Polyploidization or whole-genome duplication (WGD) is a major driving force in species diversification. Repeated WGD has been found in species-rich groups or families such as ferns, Asteraceae or Fabaceae. However, there is a paradox between the abundant species diversity of Orchidaceae and the rarely discovered WGD events. We hypothesized that it could be due to the early research strategy of a small sample size of species belonging to not closely related groups. Paphiopedilum has a rich variation on chromosome number and morphology. Here, we select it as the representative group of orchids, and use the synonymous substitution rate (K_s), phylogenomic and relative dating methods to detect whether WGD events have been occurred in P. armeniacum, P. concolor, P. hirsutissimum or P. malipoense based on the shared transcriptome data. The result shows that three WGDs are detected in all four species of Paphiopedilum, which occurred in 110.17-119.77 Mya (WGD1), 60.95-74.19 Mya (WGD2), and 38.19-45.85 Mya (WGD3), respectively. WGD3 is a newly detected whole-genome duplication event in orchids and speculated to occur after the differentiation of Cypripedioideae and its sister groups, but before the differentiation of Paphiopedilum and its sister groups. In addition, the retained duplicated genes of three WGDs are functionally related with the environmental stress response at that time. It is speculated that WGD has improved the adaptability of the ancestors of Paphiopedilum to extreme environmental changes.

Key words: polyploidization, Ochidaceae, Cypripedioideae, adaptive evolution, synonymous substitution rate

王蒙, 王婷, 夏增强, 李廷章, 金效华, 严岳鸿, 陈建兵. 基于转录组数据揭示4种兜兰的全基因组复制历史. 植物学报, 2021, 56(6): 699-714.

Meng Wang, Ting Wang, Zengqiang Xia, Tingzhang Li, Xiaohua Jin, Yuehong Yan, Jianbing Chen. Revealing the New Whole-genome Duplication Event of Four Paphiopedilum Species Based on Transcriptome Data. Chinese Bulletin of Botany, 2021, 56(6): 699-714.

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链接本文: https://www.chinbullbotany.com/CN/10.11983/CBB21100

https://www.chinbullbotany.com/CN/Y2021/V56/I6/699

图/表 9

表1 转录组原始数据和de novo组装结果

Table 1 The statistics of raw data and de novo assembly

	Paphiopedilum concolor	P. hirsutissimum	P. malipoense	P. armeniacum
Accession number	SRR1405683	SRR1405685	SRR5722160	SRR9842184
Tissues	Leaf	Leaf	Stem	Seed
Bases (Gb)	3.6	3	14.1	8
Number of transcripts	156581	76006	239105	164515
Average length of transcript (bp)	907.1	1162.3	884.5	993.2
N50 of transcript (bp)	1486	1971	1627	1856
Number of unigenes	116919	62565	201606	139203
Average length of unigene (bp)	863.3	1071.1	815.6	906.4
N50 of unigene (bp)	1438	1829	1480	1704
Source of raw data	Li et al., 2014	Li et al., 2014	Zhang et al., 2017	Fang et al., 2020

图1 BUSCO评估结果 C: 完整覆盖的基因数; S: 完整覆盖且为单拷贝的基因数; D: 完整覆盖且为多拷贝的基因数; F: 未完整覆盖的基因数; M: 缺失基因数

Figure 1 BUSCO assessment results C: Complete BUSCOs; S: Complete and single-copy BUSCOs; D: Complete and duplicated BUSCOs; F: Fragmented BUSCOs; M: Missing BUSCOs

表2 蛋白编码区和转录因子预测结果

Table 2 The summary of protein coding sequence and transcription factor prediction

	Paphiopedilum concolor	P. hirsutissimum	P. malipoense	P. armeniacum
Number of protein coding sequences	56439	33207	79854	58575
Average length of protein coding sequence (bp)	936.1	994.9	829.1	914.7
N50 of protein coding sequence (bp)	1209	1308	1089	1215
Number of CDS identified as transcription factor	1950	1181	2586	2014
Number of transcription factor families	66	67	67	68

图2 4种兜兰的Ks密度分布灰色直方图: 物种内旁系同源基因的Ks密度分布; 红色曲线: 4种兜兰与深圳拟兰间直系同源基因的Ks密度分布; 绿色曲线: 杏黄兜兰与其它3种兜兰间直系同源基因的Ks密度分布; 蓝色虚线: 物种内旁系同源基因Ks值的高斯混合模型拟合结果; 灰色虚线: 高斯混合模型显著拟合到的Ks峰值。

Figure 2 The density plot of Ks from four species of Paphiopedilum Histograms filled in grey: The density distributions of intraspecies paralogue Ks values; Red solid curves: The Ks density plots of interspecies orthologues between four species of Paphiopedilum and Apostasia shenzhenica; Green solid curves: The Ks density plots of interspecies orthologues between P. armeniacum and other three species of Paphiopedilum; Blue dashed curves: The fitting results based on Gaussian mixture modeling of intraspecies paralogue Ks values; Grey dashed lines: The Ks values of significant peaks identified by Gaussian mixture modeling.

表3 基于高斯混合模型拟合的Ks结果

Table 3 The Ks value based on Gaussian mixture modeling

Species	No. of components	No. of duplicates	BIC	Variance	Mean (K_s)	Proportion
Paphiopedilum concolor	9	207	-4673.731	0.0000	0.1077	0.0527
	9	385	-4673.731	0.0002	0.1314	0.1048
	9	416	-4673.731	0.0007	0.1740	0.1194
	9	311	-4673.731	0.0026	0.2517	0.0964
	9	522	-4673.731	0.0175	0.5161	0.1544
	9	642	-4673.731	0.0241	0.8236	0.1741
	9	567	-4673.731	0.1557	1.5043	0.1594
	9	300	-4673.731	0.5765	2.4529	0.1148
	9	90	-4673.731	0.1277	4.3036	0.0240
P. hirsutissimum	7	196	-4604.688	0.0001	0.1146	0.0632
	7	277	-4604.688	0.0005	0.1504	0.0991
	7	290	-4604.688	0.0026	0.2292	0.1109
	7	558	-4604.688	0.0282	0.5407	0.2162
	7	508	-4604.688	0.0260	0.8544	0.1693
	7	585	-4604.688	0.2594	1.5894	0.2351
	7	236	-4604.688	0.8550	3.0527	0.1062
Species	No. of components	No. of duplicates	BIC	Variance	Mean (K_s)	Proportion
P. malipoense	9	377	-14027.68	0.0000	0.1081	0.0399
	9	751	-14027.68	0.0003	0.1362	0.0890
	9	820	-14027.68	0.0016	0.2006	0.1005
	9	579	-14027.68	0.0067	0.3290	0.0768
	9	1611	-14027.68	0.0287	0.6196	0.1983
	9	1464	-14027.68	0.0447	1.0026	0.1778
	9	1634	-14027.68	0.1002	1.6186	0.1952
	9	683	-14027.68	0.5901	2.6205	0.1105
	9	105	-14027.68	0.0568	4.5773	0.0121
P. armeniacum	9	206	-8261.607	0.0000	0.1063	0.0359
	9	472	-8261.607	0.0002	0.1296	0.0870
	9	478	-8261.607	0.0008	0.1744	0.0950
	9	400	-8261.607	0.0039	0.2729	0.0849
	9	1089	-8261.607	0.0213	0.5664	0.2105
	9	778	-8261.607	0.0287	0.8825	0.1457
	9	999	-8261.607	0.1443	1.4888	0.1980
	9	455	-8261.607	0.5375	2.4393	0.1195
	9	120	-8261.607	0.1481	4.3256	0.0234

图3 基于系统发生基因组学的全基因组复制检测结果 (A) 各结点的复制基因家族情况统计, 其中Node ID对应(B)中相应结点; GD number为各结点复制基因家族数量; GD type为复制基因家族每种类型的数量; (B) 结点下方黄色方框内数字为复制基因家族的数量/基因家族的数量, 绿色方框内数字为(AB)(AB)类型复制基因家族占复制基因家族的比例; 分支上方绿色数字、下方红色数字分别表示基因家族的扩张和收缩。

Figure 3 The detection of whole-genome duplication based on phylogenomics (A) The statistics of duplicated gene families, Node ID corresponds to the node number in (B); GD number is the number of duplicated gene families at each node; GD type is the number of each type of duplicated gene families; (B) The numbers in yellow box below nodes is the number of duplicated gene families/gene families, the corresponding green box is the percentage of (AB)(AB) types; numbers above (green) and below (red) branches indicate the expansion and contraction of gene families, respectively.

表4 基于Ks峰值对全基因组复制(WGD)事件进行定年

Table 4 Dating the whole-genome duplication (WGD) event using Ks distribution peaks

Species	Name of WGD	Mean (K_s)	Age of WGD calculated by K_s mean value (Mya)	Age of WGD with 95% confidence interval (Mya)
Paphiopedilum concolor	WGD3	0.5161	38.19	37.35-39.03
	WGD2	0.8236	60.95	60.06-61.83
	WGD1	1.5043	111.32	108.91-113.72
P. hirsutissimum	WGD3	0.5407	40.01	38.98-41.04
	WGD2	0.8544	63.22	62.19-64.26
	WGD1	1.5894	117.61	114.56-120.67
P. malipoense	WGD3	0.6196	45.85	45.24-46.46
	WGD2	1.0026	74.19	73.39-74.99
	WGD1	1.6186	119.77	118.64-120.91
P. armeniacum	WGD3	0.5664	41.92	41.28-42.56
	WGD2	0.8825	65.31	64.43-66.19
	WGD1	1.4888	110.17	108.42-111.91

图4 转录组GO功能注释和复制基因功能富集的二级分类统计 Transcriptome: 转录组功能注释结果; WGD1: 全基因组复制事件WGD1中复制基因的功能富集结果(P<0.05); WGD2: 全基因组复制事件WGD2中复制基因的功能富集结果(P<0.05); WGD3: 全基因组复制事件WGD3中复制基因的功能富集结果(P<0.05); BP: 生物学过程; CC: 细胞组分; MF: 分子功能

Figure 4 The level 2 GO categories of transcriptome functional annotation and duplicated gene functional enrichment Transcriptome: Results of transcriptome functional annotation; WGD1: Functional enrichment of duplicated gene from whole- genome duplication (WGD) event WGD1 (P<0.05); WGD2: Functional enrichment of duplicated gene from WGD2 (P<0.05); WGD3: Functional enrichment of duplicated gene from WGD3 (P<0.05); BP: Biological process; CC: Cellular component; MF: Molecular function

图5 基于GO功能注释结果的3种及以上兜兰物种共同富集的GO条目 BP、CC和MF同图4。

Figure 5 The shared GO terms of 3 or more Paphiopedilum species based on the results of GO functional enrichment BP, CC, and MF see Figure 4.

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基于转录组数据揭示4种兜兰的全基因组复制历史

Revealing the New Whole-genome Duplication Event of Four Paphiopedilum Species Based on Transcriptome Data

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